Molecular Mechanisms and Evolution of Phenotypic Plasticity

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Phenotypic plasticity is used by an incredible diversity of organisms, from plants to humans. Its ubiquity attests to its fundamental importance in life. This project addresses the fascinating and understudied question of the mechanistic basis of phenotypic plasticity – i.e., how developmental processes are influenced by environmental cues to cause phenotypic differences -- and, importantly, how those processes evolve. The focus here is on an innovative model, the pea aphid, which exhibits a textbook example of phenotypic plasticity. This species offers an unparalleled opportunity to examine the role of nature and nurture in phenotype determination: it exhibits dramatically different winged and wingless morphs that are induced by environmental conditions in genetically identical, asexual females and controlled by a single genetic locus in males. Thus, strikingly, two dimorphisms, each under different control mechanisms, exist within this single species. The proposed experiments build on the exciting recent discoveries made by the PI about the role of hormones and horizontally transferred genes in the female wing plasticity and about the identification of the wing polymorphism locus in males, which has an insertion containing a duplication of a gene that influences signaling (follistatin) and which is specific to wingless males. The proposed, vigorous research program aims to decipher the molecular mechanisms underlying the function and evolution of plasticity. Experiments on the wing plasticity will examine the regulatory changes that control it, the epigenetic changes that accompany it, and test if horizontally transferred genes are preferentially recruited into the process. Experiments on the genetic male wing dimorphism will use functional and evolutionary studies of the follistatin paralogs to establish how changes in these paralogs underlie male morphological evolution. Studies in females and males will be united with experiments that will test whether or not the more recently derived male dimorphism evolved by genetic accommodation of the female plasticity, hypothesizing that males bypass the environmental signals used by the female plasticity. These studies will provide some of the first insights into the mechanistic basis of genetic accommodation, where trait variation shifts from being caused by “nurture” to “nature”. These experiments will have broad implications for understanding the mechanistic basis and evolution of plasticity, which is significant from a human health perspective because of the numerous plastic traits that influence human health and disease.